Photosynthesis Research

, 98:541 | Cite as

Heat stress: an overview of molecular responses in photosynthesis

  • Suleyman I. AllakhverdievEmail author
  • Vladimir D. Kreslavski
  • Vyacheslav V. Klimov
  • Dmitry A. Los
  • Robert Carpentier
  • Prasanna Mohanty


The primary targets of thermal damage in plants are the oxygen evolving complex along with the associated cofactors in photosystem II (PSII), carbon fixation by Rubisco and the ATP generating system. Recent investigations on the combined action of moderate light intensity and heat stress suggest that moderately high temperatures do not cause serious PSII damage but inhibit the repair of PSII. The latter largely involves de novo synthesis of proteins, particularly the D1 protein of the photosynthetic machinery that is damaged due to generation of reactive oxygen species (ROS), resulting in the reduction of carbon fixation and oxygen evolution, as well as disruption of the linear electron flow. The attack of ROS during moderate heat stress principally affects the repair system of PSII, but not directly the PSII reaction center (RC). Heat stress additionally induces cleavage and aggregation of RC proteins; the mechanisms of such processes are as yet unclear. On the other hand, membrane linked sensors seem to trigger the accumulation of compatible solutes like glycinebetaine in the neighborhood of PSII membranes. They also induce the expression of stress proteins that alleviate the ROS-mediated inhibition of repair of the stress damaged photosynthetic machinery and are required for the acclimation process. In this review we summarize the recent progress in the studies of molecular mechanisms involved during moderate heat stress on the photosynthetic machinery, especially in PSII.


Acclimation Heat stress Photosynthesis Photosystem II 



Ascorbate peroxidase






Oxygen-evolving complex


Photosynthetic machinery


Photosystem II


Photosystem I


Quantitative trait loci


Reaction center


Reactive oxygen species



This work was supported, in part, by grants from the Russian Foundation for Basic Research and from the Molecular and Cellular Biology Programs of the Russian Academy of Sciences. P.M. acknowledges the support of INSA, JNU, and DST/RAS (INT/ILTP/B-6.27). R.C. was supported by NSERC. The authors thank Dr. Anjana Jajoo for helpful discussion and reading the manuscript.


  1. Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition a historical perspective. Photosynth Res 76:343–370. doi: 10.1023/A:1024969518145 PubMedCrossRefGoogle Scholar
  2. Al-Khatib K, Paulsen GM (1989) Enhancement of thermal injury to photosynthesis in wheat plants and thylakoids by high light intensity. Plant Physiol 90:1041–1048PubMedCrossRefGoogle Scholar
  3. Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage—repair cycle of photosystem II in Synechocystis sp. PCC. 6803. Biochim Biophys Acta 1657:23–32. doi: 10.1016/j.bbabio.2004.03.003 PubMedCrossRefGoogle Scholar
  4. Allakhverdiev SI, Feyziev YM, Ahmed A, Hayashi H, Aliev JA, Klimov VV et al (1996) Stabilization of oxygen evolution and primary electron transport reactions in photosystem II against heat stress with glycinebetaine and sucrose. J Photochem Photobiol 34:149–157. doi: 10.1016/1011-1344(95)07276-4 CrossRefGoogle Scholar
  5. Allakhverdiev SI, Yruela Y, Picorel R, Klimov VV (1997) Bicarbonate is an essential constituent of the water-oxidizing complex of photosystem II. Proc Natl Acad Sci USA 94:5050–5054. doi: 10.1073/pnas.94.10.5050 PubMedCrossRefGoogle Scholar
  6. Allakhverdiev SI, Kinoshita M, Inaba M, Suzuki I, Murata N (2001) Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. Plant Physiol 125:1842–1853. doi: 10.1104/pp.125.4.1842 PubMedCrossRefGoogle Scholar
  7. Allakhverdiev SI, Hayashi H, Nishiyama Y, Ivanov AG, Aliev Ja A, Klimov VV et al (2003) Glycine betaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol 160:41–49. doi: 10.1078/0176-1617-00845 PubMedCrossRefGoogle Scholar
  8. Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis. Plant Physiol 137:263–273. doi: 10.1104/pp.104.054478 PubMedCrossRefGoogle Scholar
  9. Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767:1363–1371PubMedGoogle Scholar
  10. Allen R (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107:1049–1054PubMedGoogle Scholar
  11. Aminaka R, Taira Y, Kashino Y, Koike H, Satoh K (2006) Acclimation to the growth temperature and thermosensitivity of photosystem II in a mesophilic cyanobacterium, Synechocystis sp. PCC6803. Plant Cell Physiol 47:1612–1621. doi: 10.1093/pcp/pcl024 PubMedCrossRefGoogle Scholar
  12. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134. doi: 10.1016/0005-2728(93)90134-2 PubMedCrossRefGoogle Scholar
  13. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639. doi: 10.1146/annurev.arplant.50.1.601 PubMedCrossRefGoogle Scholar
  14. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396. doi: 10.1104/pp.106.082040 PubMedCrossRefGoogle Scholar
  15. Balint I, Bhattacharya J, Perelman A, Schatz D, Moskovitz Y, Keren N et al (2006) Inactivation of the extrinsic subunit of photosystem II, PsbU, in Synechococcus PCC 7942 results in elevated resistance to oxidative stress. FEBS Lett 580:2117–2122. doi: 10.1016/j.febslet.2006.03.020 PubMedCrossRefGoogle Scholar
  16. Barber J, Ford RC, Mitchell RAC, Millner PA (1984) Chloroplast thylakoid membrane fluidity and its sensitivity to temperature. Planta 161:375–380. doi: 10.1007/BF00398729 CrossRefGoogle Scholar
  17. Barua D, Downs CA, Hechthorn SA (2003) Variation in chloroplast small heat-shock protein function is a major determinant of variation in thermotolerance of photosynthetic electron transport among ecotypes of Chenopodium album. Funct Plant Biol 30:1071–1079. doi: 10.1071/FP03106 CrossRefGoogle Scholar
  18. Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543. doi: 10.1146/annurev.pp.31.060180.002423 CrossRefGoogle Scholar
  19. Bondarava N, Beyer P, Krieger-Liszkay A (2005) Function of the 23 kDa extrinsic protein of photosystem II as a manganese binding protein and its role in photoactivation. Biochim Biophys Acta 1708:63–70. doi: 10.1016/j.bbabio.2005.01.005 PubMedCrossRefGoogle Scholar
  20. Boyer JS (1982) Plant productivity and environment. Science 218:443–448. doi: 10.1126/science.218.4571.443 PubMedCrossRefGoogle Scholar
  21. Braun P, Greenberg BM, Scherz A (1990) D1–D2-cytochrome b559 complex from the aquatic plant Spirodela oligorchiza: correlation between complex integrity, spectroscopic properties, photochemical activity and pigment composition. Biochemistry 29:10376–10387. doi: 10.1021/bi00497a012 PubMedCrossRefGoogle Scholar
  22. Bukhov NG, Carpentier R (2000) Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves. Physiol Plant 110:279–285. doi: 10.1034/j.1399-3054.2000.110219.x CrossRefGoogle Scholar
  23. Bukhov NG, Mohanty P (1999) Elevated temperature stress effects on photosystems: characterization and evaluation of the nature of heat induced impairments. In: Singhal GS, Renger G, Sopory SK, Irrgang K-D, Govingjee (eds) Concepts in photobiology: photosynthesis and photomorphogenesis. Narosa Publishing House, New Delhi, pp 617–648Google Scholar
  24. Carpentier R (1999) Effect of high-temperature stress on the photosynthetic apparatus. In: Pessarakli M (ed) Handbook of plant and crop stress. Marcel Dekker Inc, New York, pp 337–348Google Scholar
  25. Carratu L, Franceschelli S, Pardini CL, Kobayashi GS, Horvath I, Vigh L et al (1996) Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc Natl Acad Sci USA 93:3870–3875. doi: 10.1073/pnas.93.9.3870 PubMedCrossRefGoogle Scholar
  26. Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaine and other compatible solutes. Curr Opin Plant Biol 5:250–257. doi: 10.1016/S1369-5266(02)00255-8 PubMedCrossRefGoogle Scholar
  27. Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97:13430–13435. doi: 10.1073/pnas.230451497 PubMedCrossRefGoogle Scholar
  28. Dau H, Iuzzolino L, Dittmer J (2001) The tetramanganese complex of photosystem II during its redox cycle. X-ray absorption results and mechanistic implications. Biochim Biophys Acta 1503:24–39. doi: 10.1016/S0005-2728(00)00230-9 PubMedCrossRefGoogle Scholar
  29. De Las Rivas J, Heredia P (1999) Structural predictions on the 33 kDa extrinsic protein associated with the oxygen evolving complex of photosynthetic organisms. Photosynth Res 61:11–21. doi: 10.1023/A:1006265816104 CrossRefGoogle Scholar
  30. Downs CA, Coleman JS, Heckathorn SA (1999) The chloroplast 22-kDa heat-shock protein: a lumenal protein that associates with the oxygen evolving complex and protects photosystem II during heat stress. J Plant Physiol 155:477–487Google Scholar
  31. El-Shitinawy F, Ebrahim MKH, Sewelam N, El-Shourbagy MN (2004) Activity of photosystem 2, lipid peroxidation, and the enzymatic antioxidant protective system in heat shocked barley seedlings. Photosynthetica 42:15–21. doi: 10.1023/B:PHOT.0000040564.79874.42 CrossRefGoogle Scholar
  32. Enami I, Kitamura M, Tomo T, Isokawa Y, Ohta H, Katoh S (1994) Is the primary cause of thermal inactivation of oxygen evolution in spinach PS II membranes release of the extrinsic 33 kDa protein or of Mn? Biochim Biophys Acta 1186:52–58. doi: 10.1016/0005-2728(94)90134-1 CrossRefGoogle Scholar
  33. Enami I, Kamo M, Ohta H, Takahashi S, Miura T, Kusayanagi M, Tanabe S, Kamei A, Motoki A, Hirano M, Tomo T, Satoh K (1998) Intramolecular cross-linking of the extrinsic 33-kDa protein leads to loss of oxygen evolution but not its ability of binding to photosystem II and stabilization of the manganese cluster. J Biol Chem 273:4629–4634. doi: 10.1074/jbc.273.8.4629 PubMedCrossRefGoogle Scholar
  34. Feller U, Crafts-Brandner SJ, Salvucci ME (1998) Moderately high temperatures inhibit ribulose-1,5-biphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiol 116:539–546. doi: 10.1104/pp.116.2.539 PubMedCrossRefGoogle Scholar
  35. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838. doi: 10.1126/science.1093087 PubMedCrossRefGoogle Scholar
  36. Gombos Z, Wada H, Murata N (1991) Direct evaluation of effects of fatty-acid unsaturation on the thermal properties of photosynthetic activities, as studied by mutation and transformation of Synechocystis PCC6803. Plant Cell Physiol 32:205–211Google Scholar
  37. Gombos Z, Wada H, Hideg E, Murata N (1994) The unsaturation of membrane lipids stabilizes photosynthesis against heat stress. Plant Physiol 104:563–567PubMedGoogle Scholar
  38. Gounaris K, Brain ARR, Quinn PJ, Williams WP (1983) Structural and functional changes associated with heat-induced phase separation of non-bilayer lipids in chloroplast thylakoid membranes. FEBS Lett 153:47–53. doi: 10.1016/0014-5793(83)80117-3 CrossRefGoogle Scholar
  39. Gounaris K, Brain ARR, Quinn PJ, Williams WP (1984) Structural reorganization of chloroplast thylakoid membranes in response to heat stress. Biochim Biophys Acta 766:198–208. doi: 10.1016/0005-2728(84)90232-9 CrossRefGoogle Scholar
  40. Hall AE (2001) Crop responses to environment. CRS Press LLC, Boca Raton, pp 324Google Scholar
  41. Havaux M (1993) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Environ 16:461–467. doi: 10.1111/j.1365-3040.1993.tb00893.x CrossRefGoogle Scholar
  42. Havaux M, Tardy F (1996) Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198:324–333. doi: 10.1007/BF00620047 CrossRefGoogle Scholar
  43. Havaux M, Greppin H, Strasser RJ (1991) Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light. Planta 186:88–98. doi: 10.1007/BF00201502 CrossRefGoogle Scholar
  44. Heckathorn S, Downs SA, Sharkey TD, Soleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol 116:439–444. doi: 10.1104/pp.116.1.439 PubMedCrossRefGoogle Scholar
  45. Heckathorn SA, Ryan SL, Baylis JA, Wang D, Hamilton EW, Cundiff L et al (2002) In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. Funct Plant Biol 29:933–944. doi: 10.1071/PP01191 CrossRefGoogle Scholar
  46. Hong SW, Vierling E (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J 27:25–35. doi: 10.1046/j.1365-313x.2001.01066.x PubMedCrossRefGoogle Scholar
  47. Horvath I, Glatz A, Varvasovszki V, Torok Z, Pali T, Balogh G et al (1998) Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a fluidity gene. Proc Natl Acad Sci USA 95:3513–3518. doi: 10.1073/pnas.95.7.3513 PubMedCrossRefGoogle Scholar
  48. Inaba M, Grandall P (1988) Electrolyte leakage as an indicator of high-temperature injury to harvested mature green tomatoes. J Am Soc Hortic Sci 113:96–99Google Scholar
  49. Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H et al (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278:12191–12198. doi: 10.1074/jbc.M212204200 PubMedCrossRefGoogle Scholar
  50. Kalitulo LN, Pshybutko NL, Kabashnikova LF, Jahns P (2003) Photosynthetic apparatus and high temperature: role of light. Bulg J Plant Physiol 32:281–289Google Scholar
  51. Katoh S, San Pietro A (1967) Photooxidation and reduction of cytochrome-552 and NADP photoreduction by Euglena chloroplast. Arch Biochem Biophys 121:211–219. doi: 10.1016/0003-9861(67)90026-4 PubMedCrossRefGoogle Scholar
  52. Kim K, Portis AR Jr (2004) Oxygen-dependent H2O2 production by rubisco. FEBS Lett 571:124–128. doi: 10.1016/j.febslet.2004.06.064 PubMedCrossRefGoogle Scholar
  53. Kimura A, Eaton-Rye JJ, Morita EH, Nishiyama Y, Hayashi H (2002) Protection of the oxygen-evolving machinery by the extrinsic proteins of photosystem II is also essential for development of cellular thermotolerance in Synechocystis sp. PCC 6803. Plant Cell Physiol 43:932–938. doi: 10.1093/pcp/pcf110 PubMedCrossRefGoogle Scholar
  54. Klimov VV, Baranov SV, Allakhverdiev SI (1997) Bicarbonate protects the donor side of photosystem II against photoinhibition and thermoinactivation. FEBS Lett 418:243–246. doi: 10.1016/S0014-5793(97)01392-6 PubMedCrossRefGoogle Scholar
  55. Komayama K, Khatoon M, Takenaka D, Horie J, Yamashita A, Yoshioka M et al (2007) Quality control photosystem II cleavage and aggregation of D1 protein in spinach thylakoids. Biochim Biophys Acta 1767:6830–6837Google Scholar
  56. Kreslavski VD, Khristin MS (2003) Aftereffect of heat shock on fluorescence induction and low-temperature fluorescence spectra of wheat leaves. Russ J Biophys 48:865–872Google Scholar
  57. Kreslavski VD, Balakhnina TI, Khristin MS, Bukhov NG (2001) Pretreatment of bean seedlings by choline compounds increases the resistance of photosynthetic apparatus to UV radiation and elevated temperatures. Photosynthetica 39:353–358. doi: 10.1023/A:1015174108937 CrossRefGoogle Scholar
  58. Kreslavski VD, Carpentier R, Klimov VV, Murata N, Allakhverdiev SI (2007) Molecular mechanisms of stress resistance of the photosynthetic apparatus. Membr Cell Biol 1:185–205Google Scholar
  59. Kreslavski V, Tatarinzev N, Shabnova N, Semenova G, Kosobrukhov A (2008) Characterization of the nature of photosynthetic recovery of wheat seedlings from short-time dark heat exposures and analysis of the mode of acclimation to different light intensities. J Plant Physiol. Scholar
  60. Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346. doi: 10.1093/jxb/erh237 PubMedCrossRefGoogle Scholar
  61. Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695. doi: 10.1104/pp.128.2.682 PubMedCrossRefGoogle Scholar
  62. Law R, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol 120:173–182. doi: 10.1104/pp.120.1.173 PubMedCrossRefGoogle Scholar
  63. Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142–157PubMedGoogle Scholar
  64. Maestri E, Klueva N, Perrotta C, Gullil M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol Biol 48:667–681. doi: 10.1023/A:1014826730024 PubMedCrossRefGoogle Scholar
  65. Mamedov MD, Hayashi H, Murata N (1993) Effects of glycinebetaine and unsaturation of membrane lipids on heat stability of photosynthetic electron transport and phosphorilation reactions in Synechocystis PCC 6803. Biochim Biophys Acta 1142:1–5. doi: 10.1016/0005-2728(93)90077-S CrossRefGoogle Scholar
  66. McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483. doi: 10.1021/cr0204294 PubMedCrossRefGoogle Scholar
  67. Miyake C, Okamura M (2003) Cyclic electron flow within PSII protects PSII from its photoinhibition in thylakoid membranes from spinach chloroplasts. Plant Cell Physiol 44:457–462. doi: 10.1093/pcp/pcg053 PubMedCrossRefGoogle Scholar
  68. Mohanty P, Vani B, Prakash S (2002) Elevated temperature treatment induced alteration in thylakoid membrane organization and energy distribution between the two photosystems in Pisum sativum. Z Naturforsch 57:836–842Google Scholar
  69. Mohanty P, Allakhverdiev SI, Murata N (2007) Application of low temperature during photoinhibition allows characterization of individual steps in photodamage and repair of photosystem II. Photosynth Res 94:217–234. doi: 10.1007/s11120-007-9184-y PubMedCrossRefGoogle Scholar
  70. Murata N, Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115:875–879PubMedGoogle Scholar
  71. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421. doi: 10.1016/j.bbabio.2006.11.019 PubMedCrossRefGoogle Scholar
  72. Nash D, Miyao M, Murata N (1985) Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim Biophys Acta 807:127–133. doi: 10.1016/0005-2728(85)90115-X CrossRefGoogle Scholar
  73. Neta-Sharir I, Isaacson T, Lurie S, Weiss D (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17:1829–1838. doi: 10.1105/tpc.105.031914 PubMedCrossRefGoogle Scholar
  74. Nishiyama Y, Los DA, Murata N (1999) PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol 120:301–308. doi: 10.1104/pp.120.1.301 PubMedCrossRefGoogle Scholar
  75. Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587–5594. doi: 10.1093/emboj/20.20.5587 PubMedCrossRefGoogle Scholar
  76. Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84:1–7. doi: 10.1007/s11120-004-6434-0 PubMedCrossRefGoogle Scholar
  77. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749. doi: 10.1016/j.bbabio.2006.05.013 PubMedCrossRefGoogle Scholar
  78. Nitta K, Suzuki N, Honma D, Kaneko Y, Nakamoto H (2005) Ultrastructural stability under high temperature or intensive light stress conferred by a small heat shock protein in cyanobacteria. FEBS Lett 579:1235–1242. doi: 10.1016/j.febslet.2004.12.095 PubMedCrossRefGoogle Scholar
  79. Ohnishi N, Murata N (2006) Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of D1 protein during photoinhibition in Synechococcus sp. PCC 7942. Plant Physiol 141:758–765. doi: 10.1104/pp.106.076976 PubMedCrossRefGoogle Scholar
  80. Papageorgiou GC, Murata N (1995) The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynth Res 44:243–252. doi: 10.1007/BF00048597 CrossRefGoogle Scholar
  81. Pastenes C, Horton R (1996) Effect of high temperature on photosynthesis in beans. Plant Physiol 112:1245–1251PubMedGoogle Scholar
  82. Pastori GM, Foyer CH (2002) Common components, networks and pathways of cross-tolerance to stress. The central role of “redox” and abscisic-acid-mediated controls. Plant Physiol 129:460–468. doi: 10.1104/pp.011021 PubMedCrossRefGoogle Scholar
  83. Pueyo JJ, Alfonso M, Andres C, Picorel R (2002) Increased tolerance to thermal inactivation of oxygen evolution in spinach photosystem II membranes by substitution of the extrinsic 33-kDa protein by its homologue from a thermophilic cyanobacterium. Biochim Biophys Acta 1554:22–35. doi: 10.1016/S0005-2728(02)00207-4 CrossRefGoogle Scholar
  84. Roose JL, Wegener KM, Pakrasi HB (2007) The extrinsic proteins of photosystem II. Photosynth Res 92:369–387. doi: 10.1007/s11120-006-9117-1 PubMedCrossRefGoogle Scholar
  85. Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25:163–171. doi: 10.1046/j.0016-8025.2001.00790.x PubMedCrossRefGoogle Scholar
  86. Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. Plant Physiol 134:1460–1470. doi: 10.1104/pp.103.038323 PubMedCrossRefGoogle Scholar
  87. Sato N, Sonoike K, Kawaguchi A, Tsuzuki M (1996) Contribution of lowered unsaturation levels of chloroplast lipids to high temperature tolerance of photosynthesis in Chlamydomonas reinhardtii. J Photochem Photobiol 36:333–337. doi: 10.1016/S1011-1344(96)07389-7 CrossRefGoogle Scholar
  88. Seidler A (1996) The extrinsic polypeptides of photosystem II. Biochim Biophys Acta 1277:35–60. doi: 10.1016/S0005-2728(96)00102-8 PubMedCrossRefGoogle Scholar
  89. Semenova GA (2004) Structural reorganization of thylakoid systems in response to heat treatment. Photosynthetica 42:521–527. doi: 10.1007/S11099-005-0008-z CrossRefGoogle Scholar
  90. Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ 28:269–277. doi: 10.1111/j.1365-3040.2005.01324.x CrossRefGoogle Scholar
  91. Shutova T, Kenneweg H, Buchta J, Nikitina J, Terentyev V, Chernyshov S et al (2008) The photosystem II-associated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal. EMBO J 27:782–791. doi: 10.1038/emboj.2008.12 PubMedCrossRefGoogle Scholar
  92. Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51. doi: 10.1111/j.0031-9317.2005.00582.x CrossRefGoogle Scholar
  93. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182. doi: 10.1016/j.tplants.2008.01.005 PubMedCrossRefGoogle Scholar
  94. Takahashi S, Nakamura T, Sakamizu M, van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45:251–255. doi: 10.1093/pcp/pch028 PubMedCrossRefGoogle Scholar
  95. Tanaka Y, Nishiyama Y, Murata N (2000) Acclimation of the photosynthetic machinery to high temperature in Chlamydomonas reinhardtii requires synthesis de novo of proteins encoded by the nuclear and chloroplast genomes. Plant Physiol 124:441–450. doi: 10.1104/pp.124.1.441 PubMedCrossRefGoogle Scholar
  96. Török Z, Goloubinoff P, Horvath I, Tsvetkova NM, Glatz A, Balogh G et al (2001) Synechocystis HSP17 is an amphitropic protein that stabilizes heat stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci USA 98:3098–3103. doi: 10.1073/pnas.051619498 PubMedCrossRefGoogle Scholar
  97. Vani B, Saradhi PP, Mohanty P (2001) Characterization of high temperature induced stress impairments in thylakoids of rice seedlings. Indian J Biochem Biophys 38:220–229PubMedGoogle Scholar
  98. Vigh L, Maresca B, Harwood JL (1998) Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem Sci 23:369–374. doi: 10.1016/S0968-0004(98)01279-1 PubMedCrossRefGoogle Scholar
  99. Villarejo A, Shutova T, Moskvin O, Forssen M, Klimov VV, Samuelsson G (2002) A photosystem II-associated carbonic anhydrase regulates the efficiency of photosynthetic oxygen evolution. EMBO J 21:1930–1938. doi: 10.1093/emboj/21.8.1930 PubMedCrossRefGoogle Scholar
  100. Wada H, Gombos Z, Murata N (1994) Contribution of membrane lipids to the ability of the photosynthetic machinery to tolerate temperature stress. Proc Natl Acad Sci USA 91:4273–4277. doi: 10.1073/pnas.91.10.4273 PubMedCrossRefGoogle Scholar
  101. Wahid A, Shabbir A (2005) Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycinebetaine. Plant Growth Regul 46:133–141. doi: 10.1007/s10725-005-8379-5 CrossRefGoogle Scholar
  102. Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223. doi: 10.1016/j.envexpbot.2007.05.011 CrossRefGoogle Scholar
  103. Weis E (1981) The temperature-sensitivity of dark inactivation and light activation of the ribulose-1,5-bisphosphate carboxylase in spinach chloroplasts. FEBS Lett 129:197–200. doi: 10.1016/0014-5793(81)80164-0 CrossRefGoogle Scholar
  104. Yamada M, Hidaka T, Fukamachi H (1996) Heat tolerance in leaves of tropical fruit crops as measured by chlorophyll fluorescence. Sci Hortic (Amsterdam) 67:39–48. doi: 10.1016/S0304-4238(96)00931-4 CrossRefGoogle Scholar
  105. Yamamoto H, Miyake C, Dietz K-J, Tomizawa K, Murata N, Yokota A (1999) Thioredoxin peroxidase in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 447:269–273. doi: 10.1016/S0014-5793(99)00309-9 PubMedCrossRefGoogle Scholar
  106. Yamane Y, Shikanai T, Koike H, Satoh K (2000) Reduction of QA in the dark: another cause of fluorescence Fo increases by high temperatures in higher plants. Photosynth Res 63:23–34. doi: 10.1023/A:1006350706802 PubMedCrossRefGoogle Scholar
  107. Yang X, Liang Z, Lu C (2005) Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol 138:2299–2309. doi: 10.1104/pp.105.063164 PubMedCrossRefGoogle Scholar
  108. Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y et al (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225:719–733. doi: 10.1007/s00425-006-0380-3 PubMedCrossRefGoogle Scholar
  109. Yordanov IS, Dilova R, Petkova T, Pangelova V, Goltsev V, Süss K-H (1986) Mechanisms of the temperature damage and acclimation of the photosynthetic apparatus. Photobiochem Photobiophys 12:147–155Google Scholar
  110. Yoshioka M, Uchida S, Mori H, Komayama K, Ohira S, Morita N et al (2006) Quality control of photosystem II. Cleavage of reaction center D1 protein in spinach thylakoids by FtsH protease under moderate heat stress. J Biol Chem 281:21660–21669. doi: 10.1074/jbc.M602896200 PubMedCrossRefGoogle Scholar
  111. Zharmukhamedov SK, Shirshikova GN, Maevskaya ZV, Antropova TM, Klimov VV (2007) Bicarbonate protects the water-oxidizing complex of photosystem II against thermoinactivation in intact Chlamydomonas reinhardtii cells. Russ J Plant Physiol 54:302–308. doi: 10.1134/S1021443707030028 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Suleyman I. Allakhverdiev
    • 1
    Email author
  • Vladimir D. Kreslavski
    • 1
  • Vyacheslav V. Klimov
    • 1
  • Dmitry A. Los
    • 2
  • Robert Carpentier
    • 3
  • Prasanna Mohanty
    • 4
    • 5
  1. 1.Institute of Basic Biological ProblemsRussian Academy of SciencesPushchino, Moscow RegionRussia
  2. 2.Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  3. 3.Groupe de Recherche en Biologie VégétaleUniversité du Québec à Trois-RivièresQuebecCanada
  4. 4.Regional Plant Resource CenterBhubaneswarIndia
  5. 5.Jawaharlal Nehru UniversityNew DelhiIndia

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